Massive and effective acorn dispersal into agroforestry systems by an overlooked vector, the Eurasian magpie (Pica pica)

Oak regeneration and the expansion of forested sites in Eurasia rely on acorn dispersal by animals, especially the Eurasian jay (Garrulus glandarius). However, in open agroforestry systems where jays are absent, such as old fields far from acorn sources, oak recruitment still occurs. We hypothesize that the Eurasian magpie (Pica pica), an abundant corvid in this system, substitutes the jay in its seed dispersal function. By ringing 169 magpies, video recording >7500 acorn removal events with trail cameras, and radiotagging 337 acorns, we quantified that (1) magpies cached 41–56% of the annual acorn production of Quercus ilex trees in single caches on the ground; (2) breeding pairs, and especially males, were the main acorn dispersers; (3) each breeding magpie cached 169–1372 acorns in 6 weeks; and (4) the effectiveness of dispersal (percentage of cached acorns resulting in seedlings) was 0.6–2.4%, which (5) yielded a high density of emerged seedlings (56–439 seedlings/ha). We evidence that magpie could be a key species in the regeneration of oak agroforestry mosaics because they massively and effectively dispersed acorns. However, in our particular study site, effectiveness was low probably due to herbivory and summer drought stress (i.e., a context limitation rather than an intrinsic limitation of the disperser). As the distributions of magpies and oaks overlap widely in Eurasia, effective acorn dispersal by magpies could have a significant role in largescale oak forest recovery in strongly fragmented landscapes.This study was funded by the Spanish Ministerio de Ciencia y Tecnología (CGL2014-53308-P), the REMEDINAL network of the Madrid Autonomous Government (S2013/MAE-2719 and S2018/EMT-4338), and the University of Alcalá (CCG2014/BIO-02, UAH-GP2019- 6). LMB was supported by an FPI fellowship from the Ministerio de Ciencia y Tecnología (BES-2015-075276). ABL acknowledges Juan de la Cierva postdoctoral fellowship and project RTI2018-096187-J-100 from Ministerio de Ciencia, Innovación y Universidades

Drivers of oak establishment in Mediterranean old fields from 25-year-old woodland islets planted to assist natural regeneration

14 p.Planted woodland islets can provide seeds for restoring forest ecosystems in Mediterranean old fields lacking seed sources, but other factors than seed arrival can also hinder the establishment of woody species. We experimentally examined factors affecting the emergence, survival, growth and recruitment of holm oak (Quercus ilex) seedlings juveniles from 25-year-old 100-m2 oak woodland islets planted in a Mediterranean old field. Wet springs and summers increased seedling emergence and survival. Distance to the islets per se did not affect seedling performance. However, emergence and survival increased in microsites close to the islets in less sun-exposed orientations of the islets and far from the islets in more sun-exposed orientations. Damage by wild boar reduced emergence, and unsheltered seedlings had 26% lower survival than sheltered ones, reflecting herbivory. Herb community biomass and light reduction by herbs increased with distance from nearest islet; the sparse herb cover around islets was due to competition from woodland islets, not to herbivory. There was a mismatch between the pattern of seedling survival and how the abundance of naturally recruited oaks varied with distance from the nearest islet; this suggests that other drivers can counteract the spatial pattern of seedling survival. We conclude that natural regeneration of Q. ilex in old fields from planted woodland islets is slow (5.7 seedlings ha?1 yr?1) due to acorn and seedling predation, and drought during spring and summer. Despite their small size, planted islets affected survival of oak juveniles depending on the orientation and distance relative to the islets.Ministerio de Ciencia y TecnologíaMinisterio de Ciencia e InnovaciónComunidad Autónoma de Madri

Predation and aridity slow down the spread of 21-year-old planted woodland islets in restored Mediterranean farmland

Las figuras y material suplementario que contiene el documento se localizan al final del mismo.Planted woodland islets act as sources of seed that may accelerate woodland development in extensive agricultural landscapes. We assessed a 1-ha plot that was planted with 16 100-m2 islets of holm oak Quercus ilex subsp. ballota seedlings near Toledo (Spain) in 1993. In spring 2014 we measured (1) acorn predation and (2) seedling emergence from seeded acorns at different distances from and orientations around the islets with half of the acorns protected to prevent predation, (3) survival of emerged seedlings, and (4) natural tree establishment outside of the planted islets. Most (96.9 %) unprotected acorns were removed or predated. Seedling emergence from protected acorns ranged from 42.9 % on the northern side of the islets to 13.2 % on the southern side, suggesting a less stressful microclimate on the northern side. Survival of naturally established seedlings was 28.6 % by the end of first summer; seedling mortality was chiefly due to drought (45.0 %) and herbivory (35.0 %). Density of emerged seedlings, surviving seedlings after first dry season, and established oaks >1-year old was similar at different distances from the islets. Over the 21 year time period, 58 new oak individuals >1-year old have established (an average of 3.3 established individuals per ha per year) at an average distance of 6.3 ± 5.4 m away from the closest islet. We conclude that initial oak regeneration triggered by small planted islets in Mediterranean abandoned farmland is slowed down by high acorn predation, seedling herbivory, and stressful microclimatic conditions. Regardless, these islets are a viable tool for regeneration of Mediterranean oak woodland.Projects from the Spanish Ministry of Science and Education (CGL2010-18312 and CGL2014-53308-P) and the Government of Madrid (S2013/MAE-2719, REMEDINAL-3) are currently providing financial support for this body of research. We are indebted to Aurora Mesa and Paula Meli for their help for acorn seeding and to Laura Ferna´ndez and Luis Cayuela for their input with some statistical analyses. The subject editor and two anonymous reviewers provided valuable comments on a former version of this manuscript

Linking animal behaviour and tree recruitment: Caching decisions by a scatter-hoarder corvid determine seed fate in a Mediterranean agroforestry system

1. Seed dispersal by scatter-hoarder corvids is key for the establishment of important tree species from the Holarctic region such as the walnut (Juglans regia). However, the factors that drive animal decisions to cache seeds in specific locations and the consequences of these decisions on seed fate are poorly understood. / 2. We experimentally created four distinct, replicated habitat types in a Mediterranean agricultural landscape where the Eurasian magpie (Pica pica) is a common scatter hoarder: soft bare soil; compacted bare soil; compacted soil with a dense herbaceous cover; and soft linear bare soil made up of the irrigation furrows that separated the rest of the treatments. We also experimentally placed visual landmarks (stones, sticks and bunches of dry plants) to test if magpies use them to place seed caches. Walnut dispersal from feeders to the habitats was monitored by radiotracking and camera traps. / 3. A sowing experiment simulating natural caches tested the effect of caching type on seed germination and seedling emergence. Seed mass was controlled for the dispersal and sowing experiments. / 4. Magpies selected the two habitats with soft soil, and avoided the one with compacted soil, to cache nuts. Seed mass did not affect dispersal distance, germination or emergence; however, heavier seeds were cached more often under litter and in the habitat with herbaceous cover, whereas lighter seeds were more often buried in the soft bare soil habitat. Seed burial under soil or litter determined seed fate, as there was virtually no emergence from unburied nuts. There was no evidence of any effect of the visual landmarks. / 5. Synthesis. The consequences of seed caching for seedling early establishment are driven by a fine decision-making process of the disperser. Magpies seemed to ponder the characteristics of the habitat and the seed itself to determine where and how to cache each nut. By doing so, magpies reinforced the quality of seed dispersal effectiveness, as they cached walnuts in locations that enhanced both seed survival and seedling emergence

Effective nut dispersal by magpies (Pica pica L.) in a Mediterranean agroecosystem

Scatter-hoarding animals such as corvids play a crucial role in the dispersal of nut-producing tree species. This interaction is well known for some corvids, but remains elusive for other species such as the magpie (Pica pica), an abundant corvid in agroecosystems and open landscapes of the Palearctic region. In addition, the establishment of the individual dispersed seeds—a prerequisite for determining seed-dispersal effectiveness—has never before been documented for the interaction between corvids and nut-producing trees. We analyzed walnut dispersal by magpies in an agroecosystem in southern Spain. We used several complementary approaches, including video recording nut removal from feeders, measuring dispersal distance using radio tracking (with radio transmitters placed inside nuts), and monitoring the fate of dispersed nuts to the time of seedling emergence. Magpies were shown to be highly active nut dispersers. The dispersal distance averaged 39.6 ± 4.5 m and ranged from 4.1 to 158.5 m. Some 90% of the removed walnuts were cached later, and most of these (98%) were buried in the soil or hidden under plant material. By the time of seedling emergence, ca. 33% of nuts remained at the caching location. Finally, 12% of the cached nuts germinated and 4% yielded an emerged seedling, facilitating the transition to the next regeneration stage. The results demonstrate for the first time that magpies can be an effective scatter-hoarding disperser of a nut-producing tree species, suggesting that this bird species may play a key role in the regeneration and expansion of broadleaf forests in Eurasia.Gobierno de EspañaComunidad de MadridMinisterio de Economía y Competitivida

Caching territoriality and site preferences by a scatter-hoarder drive the spatial pattern of seed dispersal and affect seedling emergence

1. For plants with seeds dispersed by scatter-hoarders, decision-making by animals when caching determines the spatial pattern of seed dispersal and lays the initial template for recruitment, driving the regeneration of many species. However, the mechanism by which animal behaviour shapes seed distributions in spatially complex landscapes is not well understood. We investigated caching territoriality and site preferences to determine the spatial pattern of seed caching at different scales and whether scatter-hoarding behaviour drives the spatial distribution of seedling emergence. 2. We used radio-tracking and automatic wildlife cameras to monitor holm oak (Quercus ilex) acorn caching by Eurasian magpies (Pica pica), who are effective scatter-hoarders in agroforestry systems. We assessed the effect of caching territories, distance to seed source, habitat, subhabitat, microsites, and caching material in the spatial pattern of acorn dispersal by magpies. In addition, we analysed the relationship between the density of cached acorns and of emerged seedlings in different habitats. 3. Breeding magpies cached the acorns inside their caching territories, where they preferred tilled areas over oak plantations and mostly avoided old fields. These differences in habitat preference were maximized at relatively short to medium dispersal distances, where most acorns were cached, and decreased or disappeared at long-distances. Within tree plantations, magpies preferred high plant-productivity sites over low productivity ones. At the finest spatial scale, magpies preferred structures built by animals, such as rabbit grit mounds and latrines and ant litter mounds, to cache the acorns. In many sites, magpies selected uncommon materials such as stones and litter to cover caches. In the subsequent spring, seedling emergence was positively correlated with acorn cache density. 4. Synthesis. Scatter-hoarding is a hierarchical process in which caching sites are selected using different criteria at different spatial scales driven by territoriality and site preferences. Territoriality constrained dispersal distance and the habitats available for acorn caching. Magpie territoriality therefore indirectly drives oak seedling emergence and can determine oak recruitment and forest regeneration.CGL2014-459 53308-P (Ministerio Ciencia y Tecnología) PID2019-106806GB-I00 (Ministerio Ciencia e Innovación) S2013/MAE-2719 and S2018/EMT-4338 (Remedinal, CAM) CCG2014/BIO-02 & GP2019-6 (UAH) BES-2015-075276(FPI, MCT

Services provided by birds (high-mobile link species) in farmland and forest mosaics: forest regeneration and plague regulation

Este trabajo ha sido financiado con fondos de los proyectos CICYT Ministerio de Educación y Ciencia (CGL2007−60533/BOS, CGL2010−18312/BOS) y del Ministerio de Economía y Competitividad (CGL2014−53308−P), de la red REMEDINAL (S−0505/AMB/ 0335, S2009 AMB−1783, S2013/MAE−2719 y TE-CM S2018/EMT- 4338), de la Universidad de Alcalá (CCG2014/BIO−002) y del MAGRAMA y la Fundación Biodiversidad a través de la Fundación Internacional para la Restauración de Ecosistemas. GGS fue financiado con una beca FPU (AP2006−00891) y SMH por una beca FPI (BES−2008−006630), ambas del Ministerio de Educación y Ciencia. LMB fue financiada por una beca FPI (BES-2015-075276) del Ministerio de Ciencia y Tecnología. NM fue financiada por una beca de la Universidad de Alcalá. ABL agradece ayudas postdoctorales Juan de la Cierva (FJCI-2015-23687) y de la Fundación Alexander von Humboldt. Agradecemos la colaboración de la Dirección Xeral de Conservación da Natureza de la Xunta de Galicia por las facilidades para desarrollar las investigaciones realizadas en esta Comunidad y de las bodegas de Abadía Retuerta y Martín Berdugo y de Haciendas Bio. Finalmente, agradecemos la contribución de un revisor anónimo que mejoró la versión original de este artículo.Los elementos que soportan las funciones y servicios de los ecosistemas son insuficientemente conocidos, mermando nuestra capacidad para planificar la conservación, restauración y manejo de los ecosistemas. Entre dichos elementos, el papel de la avifauna es especialmente relevante al ser especies de gran movilidad (high mobile link species) que conectan distintas unidades del paisaje. Este trabajo analiza servicios ecosistémicos importantes dependientes de interacciones biológicas mediadas por la avifauna en mosaicos agroforestales. Abordamos tres objetivos específicos: el papel de (1) los córvidos en la dispersión y reclutamiento de quercíneas, (2) la avifauna insectívora en la regulación de plagas en cultivos leñosos y (3) las aves rapaces en la regulación de avifauna-plaga en viñedos. Nuestros resultados evidencian que la avifauna realiza funciones y servicios claves para la regeneración forestal y la regulación de plagas en mosaicos agroforestales. Identificamos especies que se desconocía que realizaban una función relevante, en particular la urraca (Pica pica), cuya actividad resulta en una dispersión efectiva de nueces y bellotas, y el abejero europeo (Pernis apivorus), con un elevado consumo de avispa asiática (Vespa velutina). La instalación de cajas-nido en cultivos leñosos aumenta las poblaciones de aves insectívoras que regulan plagas; sin embargo, la capacidad de regulación de las plagas es moderada y depende del contexto ambiental o estudio de caso. Las rapaces diurnas existentes en los paisajes estudiados contribuyen al control de plagas agrícolas como la del estornino negro (Sturnus unicolor). Proponemos integrar los servicios que proporcionan las aves en la ordenación del territorio para alcanzar modelos de desarrollo más sostenibles.The elements that support functions and ecosystem services are not well known yet, and this gap reduces our capacity to plan the conservation, restoration, and management of ecosystems. Among these elements, the role of avifauna is especially relevant as birds are high-mobile link species that connect different landscape units. This article analyzes important ecosystem services driven by biological interactions that are mediated by birds in farmland and forest mosaics. We propose three specific goals: to assess the role of (1) corvids in the dispersal and recruitment of oak species, (2) insectivorous birds in pest regulation of woody crops, and (3) raptors in regulation of plague birds in vineyards. Our results show that the avifauna performs key functions and services for forest regeneration and pest regulation in agroforestry mosaics. We identified species that were not known to perform relevant functions, particularly the magpie (Pica pica) and its effective dispersion of nuts and acorns, and the honey buzzard (Pernis apivorus) and its high consumption of Asian black hornet (Vespa velutina). The installation of nest-boxes in woody crops increases the populations of insectivorous birds that regulate pests; however, the capacity of pest control is moderate and depends on the environmental context or case study. The diurnal raptors thriving in the studied landscapes contribute to the control of agricultural pests such as the spotless starling (Sturnus unicolor). We propose to integrate the services provided by birds in landscape planning to achieve more sustainable development systems.Financiado con fondos de los proyectos CICYT Ministerio de Educación y Ciencia (CGL2007−60533/BOS, CGL2010−18312/BOS) y del Ministerio de Economía y Competitividad (CGL2014−53308−P), de la red REMEDINAL (S−0505/AMB/ 0335, S2009 AMB−1783, S2013/MAE−2719 y TE-CM S2018/EMT- 4338), de la Universidad de Alcalá (CCG2014/BIO−002) y del MAGRAMA y la Fundación Biodiversidad a través de la Fundación Internacional para la Restauración de Ecosistemas. GGS fue financiado con una beca FPU (AP2006−00891) y SMH por una beca FPI (BES−2008−006630), ambas del Ministerio de Educación y Ciencia. LMB fue financiada por una beca FPI (BES-2015-075276) del Ministerio de Ciencia y Tecnología. NM fue financiada por una beca de la Universidad de Alcalá. ABL agradece ayudas postdoctorales Juan de la Cierva (FJCI-2015-23687) y de la Fundación Alexander von Humbold

Factores determinantes del reclutamiento de encinas (quercus ilex) en mosaicos agroforestales. Dispersión de bellotas por urracas (pica pica) y establecimiento de plántulas

La restauración forestal de tierras agrícolas abandonadas es uno de los grandes retos ecológicos que afrontan las sociedades en muchos lugares del mundo. Varios factores pueden limitar la restauración forestal de esas tierras en ambientes mediterráneos. El objetivo general de la Tesis Doctoral fue evaluar el efecto de diferentes factores que determinan el reclutamiento de encinas (Quercus ilex) en campos agrícolas abandonados, centrándose en la dispersión de bellotas por las urracas (Pica pica) y el establecimiento de plántulas de encina. Cuantificamos la capacidad de las urracas para dispersar bellotas y estudiamos el papel de sus territorios de almacenamiento y sus preferencias espaciales a distintas escalas para almacenarlas. Analizamos cómo la emergencia y la supervivencia de juveniles de encina es afectada por la depredación post-dispersiva de las bellotas, la herbivoría, la variabilidad climática interanual propia de ambientes mediterráneos, así como la orientación y la distancia a islotes forestales plantados para asistir la regeneración natural de encinares. Las urracas se llevaron más de la mitad de la producción anual de bellotas de los árboles. Los adultos reproductores fueron los individuos que más bellotas dispersaron, en espacial los machos. Un 86% de las bellotas removidas son almacenadas, llegando a almacenar un solo individuo más de 1300 bellotas durante seis semanas a una distancia media de 32,5 m. Las urracas siguieron un proceso jerárquico de toma de decisiones para seleccionar los lugares donde almacenar las bellotas. En este proceso, los territorios de almacenamiento restringieron tanto la distancia de dispersión como la disponibilidad a distintas escalas de los sitios para esconder las bellotas. A escala de hábitat seleccionaron las zonas aradas antes que los bosquetes y estos antes que los herbazales. Dentro de los bosquetes, seleccionaron las zonas con alta productividad vegetal. Seleccionaron las estructuras creadas por animales y los materiales menos comunes. La preferencia a escala de hábitat coincidió con la densidad de plántulas emergidas en los diferentes hábitats. La urraca es una dispersora masiva y efectiva de bellotas, pudiendo ser una especie clave en el reclutamiento de quercíneas en sistemas agroforestales. La territorialidad de la urraca dirige indirectamente la emergencia de plántulas de quercíneas pudiendo determinar su reclutamiento y la regeneración del bosque. El 96,9% de las bellotas sembradas sin proteger fueron depredadas. La supervivencia de las plántulas establecidas espontáneamente fue del 28.6%. Las primaveras húmedas favorecieron tanto la emergencia como la supervivencia de las plántulas, las cuales son, además, más tolerantes a la sequía estival. La emergencia y la supervivencia fue mayor en las orientaciones menos expuestas al sol que en las más expuestas, decreciendo ambas con la distancia al islote en las orientaciones menos expuestas. La biomasa de las herbáceas fue menor cerca de los islotes por la competencia de las encinas plantadas. Transcurridos 25 años desde la plantación de los islotes forestales de encina se han establecido de manera espontánea 92 nuevos individuos, con una tasa de reclutamiento de 5,7 individuos ha-1 año-1. Los islotes forestales de encina proveen las bellotas necesarias para la restauración de campos agrícolas abandonados donde los remanentes de este tipo de vegetación son escasos, aunque esta restauración es idiosincrásicamente lenta